Chromosomal Inversions and the Demography of Speciation in Drosophila montana and Drosophila flavomontana.

Chromosomal inversions may play a central role in speciation given their ability to locally reduce recombination and therefore genetic exchange between diverging populations. We analyzed long- and short-read whole-genome data from sympatric and allopatric populations of 2 Drosophila virilis group species, Drosophila montana and Drosophila flavomontana, to understand if inversions have contributed to their divergence. We identified 3 large alternatively fixed inversions on the X chromosome and one on each of the autosomes 4 and 5. A comparison of demographic models estimated for inverted and noninverted (colinear) chromosomal regions suggests that these inversions arose before the time of the species split. We detected a low rate of interspecific gene flow (introgression) from D. montana to D. flavomontana, which was further reduced inside inversions and was lower in allopatric than in sympatric populations. Together, these results suggest that the inversions were already present in the common ancestral population and that gene exchange between the sister taxa was reduced within inversions both before and after the onset of species divergence. Such ancestrally polymorphic inversions may foster speciation by allowing the accumulation of genetic divergence in loci involved in adaptation and reproductive isolation inside inversions early in the speciation process, while gene exchange at colinear regions continues until the evolving reproductive barriers complete speciation. The overlapping X inversions are particularly good candidates for driving the speciation process of D. montana and D. flavomontana, since they harbor strong genetic incompatibilities that were detected in a recent study of experimental introgression.

Demographically explicit scans for barriers to gene flow using gIMble.

Identifying regions of the genome that act as barriers to gene flow between recently diverged taxa has remained challenging given the many evolutionary forces that generate variation in genetic diversity and divergence along the genome, and the stochastic nature of this variation. Progress has been impeded by a conceptual and methodological divide between analyses that infer the demographic history of speciation and genome scans aimed at identifying locally maladaptive alleles i.e. genomic barriers to gene flow. Here we implement genomewide IM blockwise likelihood estimation (gIMble), a composite likelihood approach for the quantification of barriers, that bridges this divide. This analytic framework captures background selection and selection against barriers in a model of isolation with migration (IM) as heterogeneity in effective population size (Ne) and effective migration rate (me), respectively. Variation in both effective demographic parameters is estimated in sliding windows via pre-computed likelihood grids. gIMble includes modules for pre-processing/filtering of genomic data and performing parametric bootstraps using coalescent simulations. To demonstrate the new approach, we analyse data from a well-studied pair of sister species of tropical butterflies with a known history of post-divergence gene flow: Heliconius melpomene and H. cydno. Our analyses uncover both large-effect barrier loci (including well-known wing-pattern genes) and a genome-wide signal of a polygenic barrier architecture.

Do chromosome rearrangements fix by genetic drift or natural selection? Insights from Brenthis butterflies.

Large-scale chromosome rearrangements, such as fissions and fusions, are a common feature of eukaryote evolution. They can have considerable influence on the evolution of populations, yet it remains unclear exactly how rearrangements become established and eventually fix. Rearrangements could fix by genetic drift if they are weakly deleterious or neutral, or they may instead be favoured by positive natural selection. Here, we compare genome assemblies of three closely related Brenthis butterfly species and characterize a complex history of fission and fusion rearrangements. An inferred demographic history of these species suggests that rearrangements became fixed in populations with large long-term effective size (Ne ), consistent with rearrangements being selectively neutral or only very weakly underdominant. Using a recently developed analytic framework for characterizing hard selective sweeps, we find that chromosome fusions are not enriched for evidence of past sweeps compared to other regions of the genome. Nonetheless, we do infer a strong and recent selective sweep around one chromosome fusion in the B. daphne genome. Our results suggest that rearrangements in these species likely have weak absolute fitness effects and fix by genetic drift. However, one putative selective sweep raises the possibility that natural selection may sometimes play a role in the fixation of chromosome fusions.

The genome sequence of the Large Skipper, Ochlodes sylvanus, (Esper, 1777).

We present a genome assembly from an individual female Ochlodes sylvanus, the Large Skipper (Arthropoda; Insecta; Lepidoptera; Hesperiidae). The genome sequence is 380 megabases in span. Most of the assembly (99.97%) is scaffolded into 30 chromosomal pseudomolecules, including the assembled W and Z sex chromosomes. The mitochondrial genome has also been assembled and is 17.1 kilobases in length. Gene annotation of this assembly on Ensembl identified 13,451 protein coding genes.

Chromosome Fissions and Fusions Act as Barriers to Gene Flow between Brenthis Fritillary Butterflies.

Chromosome rearrangements are thought to promote reproductive isolation between incipient species. However, it is unclear how often, and under what conditions, fission and fusion rearrangements act as barriers to gene flow. Here we investigate speciation between two largely sympatric fritillary butterflies, Brenthis daphne and Brenthis ino. We use a composite likelihood approach to infer the demographic history of these species from whole-genome sequence data. We then compare chromosome-level genome assemblies of individuals from each species and identify a total of nine chromosome fissions and fusions. Finally, we fit a demographic model where effective population sizes and effective migration rate vary across the genome, allowing us to quantify the effects of chromosome rearrangements on reproductive isolation. We show that chromosomes involved in rearrangements experienced less effective migration since the onset of species divergence and that genomic regions near rearrangement points have a further reduction in effective migration rate. Our results suggest that the evolution of multiple rearrangements in the B. daphne and B. ino populations, including alternative fusions of the same chromosomes, have resulted in a reduction in gene flow. Although fission and fusion of chromosomes are unlikely to be the only processes that have led to speciation between these butterflies, this study shows that these rearrangements can directly promote reproductive isolation and may be involved in speciation when karyotypes evolve quickly.

Experimental introgression in Drosophila: Asymmetric postzygotic isolation associated with chromosomal inversions and an incompatibility locus on the X chromosome.

Interspecific gene flow (introgression) is an important source of new genetic variation, but selection against it can reinforce reproductive barriers between interbreeding species. We used an experimental approach to trace the role of chromosomal inversions and incompatibility genes in preventing introgression between two partly sympatric Drosophila virilis group species, D. flavomontana and D. montana. We backcrossed F1 hybrid females from a cross between D. flavomontana female and D. montana male with the males of the parental species for two generations and sequenced pools of parental strains and their reciprocal second generation backcross (BC2 mon and BC2 fla) females. Contrasting the observed amount of introgression (mean hybrid index, HI) in BC2 female pools along the genome to simulations under different scenarios allowed us to identify chromosomal regions of restricted and increased introgression. We found no deviation from the HI expected under a neutral null model for any chromosome for the BC2 mon pool, suggesting no evidence for genetic incompatibilities in backcrosses towards D. montana. In contrast, the BC2 fla pool showed high variation in the observed HI between different chromosomes, and massive reduction of introgression on the X chromosome (large X-effect). This observation is compatible with reduced recombination combined with at least one dominant incompatibility locus residing within the X inversion(s). Overall, our study suggests that genetic incompatibilities arising within chromosomal inversions can play an important role in speciation.

The genome sequence of the Brown Argus, Aricia agestis (Denis & Schiffermüller, 1775).

We present genome assemblies from two male Aricia agestis specimens (the Brown Argus; Arthropoda; Insecta; Lepidoptera; Lycaenidae). The genome sequences are 435.3 and 437.4 megabases in span. Each assembly is scaffolded into 23 chromosomal pseudomolecules, including the Z sex chromosome. The mitochondrial genomes were assembled and are 15.47 and 15.45 kilobases in length. Gene annotation of these assemblies on Ensembl identified 12,688 and 12,654 protein coding genes.

The genome sequence of the Chalkhill Blue, Lysandra coridon (Poda, 1761).

We present a genome assembly from an individual male Lysandra coridon (the Chalkhill Blue; Arthropoda; Insecta; Lepidoptera; Lycaenidae). The genome sequence is 541 megabases in span. Most of the assembly is scaffolded into 90 chromosomal pseudomolecules, including the assembled Z sex chromosome. The mitochondrial genome has also been assembled and is 15.4 kilobases in length. Gene annotation of this assembly on Ensembl identified 13,334 protein coding genes.

The genome sequence of the Mazarine Blue, Cyaniris semiargus (Rottemburg, 1775).

We present a genome assembly from an individual male Cyaniris semiargus (the Mazarine Blue; Arthropoda; Insecta; Lepidoptera; Lycaenidae). The genome sequence is 441.5 megabases in span. Most of the assembly is scaffolded into 24 chromosomal pseudomolecules, including the assembled Z sex chromosome. The mitochondrial genome has also been assembled and is 15.4 kilobases in length. Gene annotation of this assembly on Ensembl identified 16,408 protein coding genes.

The genome sequence of the small pearl-bordered fritillary butterfly, Boloria selene (Schiffermüller, 1775).

We present a genome assembly from an individual female Boloria selene (the small pearl-bordered fritillary, also known as the silver meadow fritillary; Arthropoda; Insecta; Lepidoptera; Nymphalidae). The genome sequence is 400 megabases in span. The complete assembly is scaffolded into 31 chromosomal pseudomolecules, with the W and Z sex chromosome assembled.

The genome sequence of the orange-tip butterfly, Anthocharis cardamines (Linnaeus, 1758).

We present a genome assembly from an individual female Anthocharis cardamines (the orange-tip; Arthropoda; Insecta; Lepidoptera; Pieridae). The genome sequence is 360 megabases in span. The majority (99.74%) of the assembly is scaffolded into 31 chromosomal pseudomolecules, with the W and Z sex chromosomes assembled. Gene annotation of this assembly on Ensembl has identified 12,477 protein coding genes.

The genome sequence of the scotch argus butterfly, Erebia aethiops (Esper, 1777).

We present a genome assembly from an individual female Erebia aethiops (the scotch argus; Arthropoda; Insecta; Lepidoptera; Nymphalidae). The genome sequence is 473 megabases in span. The complete assembly is scaffolded into 20 chromosomal pseudomolecules, with the W and Z sex chromosomes assembled. The complete mitochondrial genome was also assembled and is 15.2 kilobases in length.

The genome sequence of the scarce swallowtail, Iphiclides podalirius.

The scarce swallowtail, Iphiclides podalirius (Linnaeus, 1758), is a species of butterfly in the family Papilionidae. Here, we present a chromosome-level genome assembly for Iphiclides podalirius as well as gene and transposable element annotations. We investigate how the density of genomic features differs between the 30 Iphiclides podalirius chromosomes. We find that shorter chromosomes have higher heterozygosity at four-fold-degenerate sites and a greater density of transposable elements. While the first result is an expected consequence of differences in recombination rate, the second suggests a counter-intuitive relationship between recombination and transposable element evolution. This high-quality genome assembly, the first for any species in the tribe Leptocircini, will be a valuable resource for population genomics in the genus Iphiclides and comparative genomics more generally.

The genome sequence of the grizzled skipper, Pyrgus malvae (Linnaeus, 1758).

We present a genome assembly from an individual male Pyrgus malvae (the grizzled skipper; Arthropoda; Insecta; Lepidoptera; Hesperiidae). The genome sequence is 725 megabases in span. The majority (99.97%) of the assembly is scaffolded into 31 chromosomal pseudomolecules, with the Z sex chromosome assembled.

Estimating the rates of crossover and gene conversion from individual genomes.

Recombination can occur either as a result of crossover or gene conversion events. Population genetic methods for inferring the rate of recombination from patterns of linkage disequilibrium generally assume a simple model of recombination that only involves crossover events and ignore gene conversion. However, distinguishing the 2 processes is not only necessary for a complete description of recombination, but also essential for understanding the evolutionary consequences of inversions and other genomic partitions in which crossover (but not gene conversion) is reduced. We present heRho, a simple composite likelihood scheme for coestimating the rate of crossover and gene conversion from individual diploid genomes. The method is based on analytic results for the distance-dependent probability of heterozygous and homozygous states at 2 loci. We apply heRho to simulations and data from the house mouse Mus musculus castaneus, a well-studied model. Our analyses show (1) that the rates of crossover and gene conversion can be accurately coestimated at the level of individual chromosomes and (2) that previous estimates of the population scaled rate of recombination ρ=4Ner under a pure crossover model are likely biased.

The genome sequence of the lesser marbled fritillary, Brenthis ino, and evidence for a segregating neo-Z chromosome.

The lesser marbled fritillary, Brenthis ino (Rottemburg, 1775), is a species of Palearctic butterfly. Male Brenthis ino individuals have been reported to have between 12 and 14 pairs of chromosomes, a much-reduced chromosome number than is typical in butterflies. Here, we present a chromosome-level genome assembly for Brenthis ino, as well as gene and transposable element annotations. The assembly is 411.8 Mb in length with a contig N50 of 9.6 Mb and a scaffold N50 of 29.5 Mb. We also show evidence that the male individual from which we generated HiC data was heterozygous for a neo-Z chromosome, consistent with inheriting 14 chromosomes from one parent and 13 from the other. This genome assembly will be a valuable resource for studying chromosome evolution in Lepidoptera, as well as for comparative and population genomics more generally.

The genome sequence of the high brown fritillary, Fabriciana adippe (Dennis & Schiffermüller, 1775).

We present a genome assembly from an individual female Fabriciana adippe (the high brown fritillary; Arthropoda; Insecta; Lepidoptera; Nymphalidae). The genome sequence is 485 megabases in span. Most of the assembly (99.98%) is scaffolded into 29 chromosomal pseudomolecules with the Z sex chromosome assembled. The complete mitochondrial genome was also assembled and is 15.1 kilobases in length. Gene annotation of this assembly in Ensembl identified 13,536 protein coding genes.

The genome sequence of the Arran brown, Erebia ligea (Linnaeus, 1758).

We present a genome assembly from an individual male Erebia ligea (Arran brown; Arthropoda; Insecta; Lepidoptera; Nymphalidae). The genome sequence is 506 megabases in span. The majority (99.92%) of the assembly is scaffolded into 29 chromosomal pseudomolecules, with the Z sex chromosome assembled. The complete mitochondrial genome was also assembled and is 15.2 kilobases in length.

The genome sequence of the northern brown argus, Aricia artaxerxes (Fabricius, 1793).

We present a genome assembly from an individual Aricia artaxerxes (the northern brown argus; Arthropoda; Insecta; Lepidoptera; Lycaenidae). The genome sequence is 458 megabases in span. Most of the assembly (99.99%) is scaffolded into 23 chromosomal pseudomolecules, including the assembled Z sex chromosome. The mitochondrial genome has also been assembled and is 15.8 kilobases in length. Gene annotation of this assembly on Ensembl has identified 12,688 protein coding genes.

The genome sequence of the wood white butterfly, Leptidea sinapis (Linnaeus, 1758).

We present a genome assembly from an individual male Leptidea sinapis (the wood white; Arthropoda; Insecta; Lepidoptera; Pieridae). The genome sequence is 686 megabases in span. The majority (99.99%) of the assembly is scaffolded into 48 chromosomal pseudomolecules, with three Z sex chromosomes assembled. Gene annotation of this assembly on Ensembl has identified 14,800 protein coding genes.